Abstract
We have adapted a murine model of heterotypic rotavirus infection for the purpose of evaluating the intestinal antibody response to an infection that mimics human vaccination. Neonatal mice were infected with the rhesus rotavirus (RRV). The enzyme-linked immunospot assay was used in order to avoid common artifacts in the quantitation of intestinal immune responses inherent in measurements of luminal or serum immunoglobulins and to obtain easily quantifiable data in a flexible and convenient format. Functionally active lymphocytes were harvested from the spleen, small intestinal lamina propria, Peyer's patches, and mesenteric lymph nodes and processed into single-cell suspensions. Antibody-secreting cells (ASC) were quantitated from 5 to 50 days after infection for total, RRV-specific, baculovirus-expressed VP4-specific, and single-shell RRV-specific ASC secreting either immunoglobulin G (IgG), IgM, or IgA. The response to VP4 constituted less than 1.5% of the total virus-specific response, which was located almost exclusively in the gut and was 90% IgA. Intestinal ASC were directed overwhelmingly toward proteins incorporated in the single-shell particle, predominantly VP2 and VP6. We conclude that the antibody response to VP4, thought to be the site of the important neutralization sites conserved among several rotavirus serotypes, is an extremely small portion of the overall antibody response in the intestinal tract.
Full text
PDFSelected References
These references are in PubMed. This may not be the complete list of references from this article.
- Appleby P., Catty D. Transmission of immunoglobulin to foetal and neonatal mice. J Reprod Immunol. 1983 Jul;5(4):203–213. doi: 10.1016/0165-0378(83)90236-x. [DOI] [PubMed] [Google Scholar]
- Besser T. E., Gay C. C., McGuire T. C., Evermann J. F. Passive immunity to bovine rotavirus infection associated with transfer of serum antibody into the intestinal lumen. J Virol. 1988 Jul;62(7):2238–2242. doi: 10.1128/jvi.62.7.2238-2242.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bland P. W., Warren L. G. Antigen presentation by epithelial cells of the rat small intestine. I. Kinetics, antigen specificity and blocking by anti-Ia antisera. Immunology. 1986 May;58(1):1–7. [PMC free article] [PubMed] [Google Scholar]
- Bleicher P. A., Balk S. P., Hagen S. J., Blumberg R. S., Flotte T. J., Terhorst C. Expression of murine CD1 on gastrointestinal epithelium. Science. 1990 Nov 2;250(4981):679–682. doi: 10.1126/science.1700477. [DOI] [PubMed] [Google Scholar]
- Brüssow H., Hilpert H., Walther I., Sidoti J., Mietens C., Bachmann P. Bovine milk immunoglobulins for passive immunity to infantile rotavirus gastroenteritis. J Clin Microbiol. 1987 Jun;25(6):982–986. doi: 10.1128/jcm.25.6.982-986.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brüssow H., Offit P. A., Gerna G., Bruttin A., Sidoti J. Polypeptide specificity of antiviral serum antibodies in children naturally infected with human rotavirus. J Virol. 1990 Sep;64(9):4130–4136. doi: 10.1128/jvi.64.9.4130-4136.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buller C. R., Moxley R. A. Natural infection of porcine ileal dome M cells with rotavirus and enteric adenovirus. Vet Pathol. 1988 Nov;25(6):516–517. doi: 10.1177/030098588802500616. [DOI] [PubMed] [Google Scholar]
- Caust J., Dyall-Smith M. L., Lazdins I., Holmes I. H. Glycosylation, an important modifier of rotavirus antigenicity. Arch Virol. 1987;96(3-4):123–134. doi: 10.1007/BF01320955. [DOI] [PubMed] [Google Scholar]
- Cerf-Bensussan N., Quaroni A., Kurnick J. T., Bhan A. K. Intraepithelial lymphocytes modulate Ia expression by intestinal epithelial cells. J Immunol. 1984 May;132(5):2244–2252. [PubMed] [Google Scholar]
- Chen K. S., Strober W. Cholera holotoxin and its B subunit enhance Peyer's patch B cell responses induced by orally administered influenza virus: disproportionate cholera toxin enhancement of the IgA B cell response. Eur J Immunol. 1990 Feb;20(2):433–436. doi: 10.1002/eji.1830200230. [DOI] [PubMed] [Google Scholar]
- Christy C., Madore H. P., Pichichero M. E., Gala C., Pincus P., Vosefski D., Hoshino Y., Kapikian A., Dolin R. Field trial of rhesus rotavirus vaccine in infants. Pediatr Infect Dis J. 1988 Sep;7(9):645–650. doi: 10.1097/00006454-198809000-00009. [DOI] [PubMed] [Google Scholar]
- Coulson B. S., Tursi J. M., McAdam W. J., Bishop R. F. Derivation of neutralizing monoclonal antibodies to human rotaviruses and evidence that an immunodominant neutralization site is shared between serotypes 1 and 3. Virology. 1986 Oct 30;154(2):302–312. doi: 10.1016/0042-6822(86)90456-3. [DOI] [PubMed] [Google Scholar]
- Czerkinsky C. C., Nilsson L. A., Nygren H., Ouchterlony O., Tarkowski A. A solid-phase enzyme-linked immunospot (ELISPOT) assay for enumeration of specific antibody-secreting cells. J Immunol Methods. 1983 Dec 16;65(1-2):109–121. doi: 10.1016/0022-1759(83)90308-3. [DOI] [PubMed] [Google Scholar]
- Dharakul T., Riepenhoff-Talty M., Albini B., Ogra P. L. Distribution of rotavirus antigen in intestinal lymphoid tissues: potential role in development of the mucosal immune response to rotavirus. Clin Exp Immunol. 1988 Oct;74(1):14–19. [PMC free article] [PubMed] [Google Scholar]
- Estes M. K., Cohen J. Rotavirus gene structure and function. Microbiol Rev. 1989 Dec;53(4):410–449. doi: 10.1128/mr.53.4.410-449.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Estes M. K., Graham D. Y., Smith E. M., Gerba C. P. Rotavirus stability and inactivation. J Gen Virol. 1979 May;43(2):403–409. doi: 10.1099/0022-1317-43-2-403. [DOI] [PubMed] [Google Scholar]
- Flores J., Daoud G., Daoud N., Puig M., Martinez M., Perez-Schael I., Shaw R., Greenberg H. B., Midthun K., Kapikian A. Z. Reactogenicity and antigenicity of rhesus rotavirus vaccine (MMU-18006) in newborn infants in Venezuela. Pediatr Infect Dis J. 1988 Nov;7(11):776–780. doi: 10.1097/00006454-198811000-00006. [DOI] [PubMed] [Google Scholar]
- Flores J., Perez-Schael I., Gonzalez M., Garcia D., Perez M., Daoud N., Cunto W., Chanock R. M., Kapikian A. Z. Protection against severe rotavirus diarrhoea by rhesus rotavirus vaccine in Venezuelan infants. Lancet. 1987 Apr 18;1(8538):882–884. doi: 10.1016/s0140-6736(87)92858-3. [DOI] [PubMed] [Google Scholar]
- Fuhrman J. A., Cebra J. J. Special features of the priming process for a secretory IgA response. B cell priming with cholera toxin. J Exp Med. 1981 Mar 1;153(3):534–544. doi: 10.1084/jem.153.3.534. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Green K. Y., Taniguchi K., Mackow E. R., Kapikian A. Z. Homotypic and heterotypic epitope-specific antibody responses in adult and infant rotavirus vaccinees: implications for vaccine development. J Infect Dis. 1990 Apr;161(4):667–679. doi: 10.1093/infdis/161.4.667. [DOI] [PubMed] [Google Scholar]
- Greenberg H. B., Valdesuso J., van Wyke K., Midthun K., Walsh M., McAuliffe V., Wyatt R. G., Kalica A. R., Flores J., Hoshino Y. Production and preliminary characterization of monoclonal antibodies directed at two surface proteins of rhesus rotavirus. J Virol. 1983 Aug;47(2):267–275. doi: 10.1128/jvi.47.2.267-275.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Greenberg H. B., Vo P. T., Jones R. Cultivation and characterization of three strains of murine rotavirus. J Virol. 1986 Feb;57(2):585–590. doi: 10.1128/jvi.57.2.585-590.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hoshino Y., Saif L. J., Sereno M. M., Chanock R. M., Kapikian A. Z. Infection immunity of piglets to either VP3 or VP7 outer capsid protein confers resistance to challenge with a virulent rotavirus bearing the corresponding antigen. J Virol. 1988 Mar;62(3):744–748. doi: 10.1128/jvi.62.3.744-748.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hoshino Y., Sereno M. M., Midthun K., Flores J., Kapikian A. Z., Chanock R. M. Independent segregation of two antigenic specificities (VP3 and VP7) involved in neutralization of rotavirus infectivity. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8701–8704. doi: 10.1073/pnas.82.24.8701. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ijaz M. K., Dent D., Haines D., Babiuk L. A. Development of a murine model to study the pathogenesis of rotavirus infection. Exp Mol Pathol. 1989 Oct;51(2):186–204. doi: 10.1016/0014-4800(89)90019-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kalica A. R., Flores J., Greenberg H. B. Identification of the rotaviral gene that codes for hemagglutination and protease-enhanced plaque formation. Virology. 1983 Feb;125(1):194–205. doi: 10.1016/0042-6822(83)90073-9. [DOI] [PubMed] [Google Scholar]
- Kalica A. R., Greenberg H. B., Wyatt R. G., Flores J., Sereno M. M., Kapikian A. Z., Chanock R. M. Genes of human (strain Wa) and bovine (strain UK) rotaviruses that code for neutralization and subgroup antigens. Virology. 1981 Jul 30;112(2):385–390. doi: 10.1016/0042-6822(81)90285-3. [DOI] [PubMed] [Google Scholar]
- Kaljot K. T., Shaw R. D., Rubin D. H., Greenberg H. B. Infectious rotavirus enters cells by direct cell membrane penetration, not by endocytosis. J Virol. 1988 Apr;62(4):1136–1144. doi: 10.1128/jvi.62.4.1136-1144.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kapikian A. Z., Flores J., Hoshino Y., Glass R. I., Midthun K., Gorziglia M., Chanock R. M. Rotavirus: the major etiologic agent of severe infantile diarrhea may be controllable by a "Jennerian" approach to vaccination. J Infect Dis. 1986 May;153(5):815–822. doi: 10.1093/infdis/153.5.815. [DOI] [PubMed] [Google Scholar]
- Lazdins I., Sonza S., Dyall-Smith M. L., Coulson B. S., Holmes I. H. Demonstration of an immunodominant neutralization site by analysis of antigenic variants of SA11 rotavirus. J Virol. 1985 Oct;56(1):317–319. doi: 10.1128/jvi.56.1.317-319.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu M., Offit P. A., Estes M. K. Identification of the simian rotavirus SA11 genome segment 3 product. Virology. 1988 Mar;163(1):26–32. doi: 10.1016/0042-6822(88)90230-9. [DOI] [PubMed] [Google Scholar]
- Mackow E. R., Barnett J. W., Chan H., Greenberg H. B. The rhesus rotavirus outer capsid protein VP4 functions as a hemagglutinin and is antigenically conserved when expressed by a baculovirus recombinant. J Virol. 1989 Apr;63(4):1661–1668. doi: 10.1128/jvi.63.4.1661-1668.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mackow E. R., Shaw R. D., Matsui S. M., Vo P. T., Benfield D. A., Greenberg H. B. Characterization of homotypic and heterotypic VP7 neutralization sites of rhesus rotavirus. Virology. 1988 Aug;165(2):511–517. doi: 10.1016/0042-6822(88)90595-8. [DOI] [PubMed] [Google Scholar]
- Mackow E. R., Vo P. T., Broome R., Bass D., Greenberg H. B. Immunization with baculovirus-expressed VP4 protein passively protects against simian and murine rotavirus challenge. J Virol. 1990 Apr;64(4):1698–1703. doi: 10.1128/jvi.64.4.1698-1703.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mackow E. R., Yamanaka M. Y., Dang M. N., Greenberg H. B. DNA amplification-restricted transcription-translation: rapid analysis of rhesus rotavirus neutralization sites. Proc Natl Acad Sci U S A. 1990 Jan;87(2):518–522. doi: 10.1073/pnas.87.2.518. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Matsui S. M., Mackow E. R., Greenberg H. B. Molecular determinant of rotavirus neutralization and protection. Adv Virus Res. 1989;36:181–214. doi: 10.1016/s0065-3527(08)60585-0. [DOI] [PubMed] [Google Scholar]
- Matsui S. M., Offit P. A., Vo P. T., Mackow E. R., Benfield D. A., Shaw R. D., Padilla-Noriega L., Greenberg H. B. Passive protection against rotavirus-induced diarrhea by monoclonal antibodies to the heterotypic neutralization domain of VP7 and the VP8 fragment of VP4. J Clin Microbiol. 1989 Apr;27(4):780–782. doi: 10.1128/jcm.27.4.780-782.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mayer L., Shlien R. Evidence for function of Ia molecules on gut epithelial cells in man. J Exp Med. 1987 Nov 1;166(5):1471–1483. doi: 10.1084/jem.166.5.1471. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Momburg F., Koretz K., Von Herbay A., Möller P. Nonimmune human cells can express MHC class II antigens in the absence of invariant chain--an immunohistological study on normal and chronically inflamed small intestine. Clin Exp Immunol. 1988 Jun;72(3):367–372. [PMC free article] [PubMed] [Google Scholar]
- Offit P. A., Blavat G. Identification of the two rotavirus genes determining neutralization specificities. J Virol. 1986 Jan;57(1):376–378. doi: 10.1128/jvi.57.1.376-378.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Offit P. A., Clark H. F., Blavat G., Greenberg H. B. Reassortant rotaviruses containing structural proteins vp3 and vp7 from different parents induce antibodies protective against each parental serotype. J Virol. 1986 Nov;60(2):491–496. doi: 10.1128/jvi.60.2.491-496.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Offit P. A., Clark H. F., Kornstein M. J., Plotkin S. A. A murine model for oral infection with a primate rotavirus (simian SA11). J Virol. 1984 Jul;51(1):233–236. doi: 10.1128/jvi.51.1.233-236.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Offit P. A., Clark H. F. Maternal antibody-mediated protection against gastroenteritis due to rotavirus in newborn mice is dependent on both serotype and titer of antibody. J Infect Dis. 1985 Dec;152(6):1152–1158. doi: 10.1093/infdis/152.6.1152. [DOI] [PubMed] [Google Scholar]
- Offit P. A., Clark H. F. Protection against rotavirus-induced gastroenteritis in a murine model by passively acquired gastrointestinal but not circulating antibodies. J Virol. 1985 Apr;54(1):58–64. doi: 10.1128/jvi.54.1.58-64.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Offit P. A., Dudzik K. I. Rotavirus-specific cytotoxic T lymphocytes appear at the intestinal mucosal surface after rotavirus infection. J Virol. 1989 Aug;63(8):3507–3512. doi: 10.1128/jvi.63.8.3507-3512.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Offit P. A., Shaw R. D., Greenberg H. B. Passive protection against rotavirus-induced diarrhea by monoclonal antibodies to surface proteins vp3 and vp7. J Virol. 1986 May;58(2):700–703. doi: 10.1128/jvi.58.2.700-703.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Owen R. L., Jones A. L. Epithelial cell specialization within human Peyer's patches: an ultrastructural study of intestinal lymphoid follicles. Gastroenterology. 1974 Feb;66(2):189–203. [PubMed] [Google Scholar]
- Owen R. L., Pierce N. F., Apple R. T., Cray W. C., Jr M cell transport of Vibrio cholerae from the intestinal lumen into Peyer's patches: a mechanism for antigen sampling and for microbial transepithelial migration. J Infect Dis. 1986 Jun;153(6):1108–1118. doi: 10.1093/infdis/153.6.1108. [DOI] [PubMed] [Google Scholar]
- Owen R. L. Sequential uptake of horseradish peroxidase by lymphoid follicle epithelium of Peyer's patches in the normal unobstructed mouse intestine: an ultrastructural study. Gastroenterology. 1977 Mar;72(3):440–451. [PubMed] [Google Scholar]
- Ramig R. F. The effects of host age, virus dose, and virus strain on heterologous rotavirus infection of suckling mice. Microb Pathog. 1988 Mar;4(3):189–202. doi: 10.1016/0882-4010(88)90069-1. [DOI] [PubMed] [Google Scholar]
- Rennels M. B., Losonsky G. A., Levine M. M., Kapikian A. Z. Preliminary evaluation of the efficacy of rhesus rotavirus vaccine strain MMU 18006 in young children. Pediatr Infect Dis. 1986 Sep-Oct;5(5):587–588. doi: 10.1097/00006454-198609000-00019. [DOI] [PubMed] [Google Scholar]
- Rennels M. B., Losonsky G. A., Young A. E., Shindledecker C. L., Kapikian A. Z., Levine M. M. An efficacy trial of the rhesus rotavirus vaccine in Maryland. The Clinical Study Group. Am J Dis Child. 1990 May;144(5):601–604. doi: 10.1001/archpedi.1990.02150290095037. [DOI] [PubMed] [Google Scholar]
- Shaw R. D., Fong K. J., Losonsky G. A., Levine M. M., Maldonado Y., Yolken R., Flores J., Kapikian A. Z., Vo P. T., Greenberg H. B. Epitope-specific immune responses to rotavirus vaccination. Gastroenterology. 1987 Nov;93(5):941–950. doi: 10.1016/0016-5085(87)90555-5. [DOI] [PubMed] [Google Scholar]
- Shaw R. D., Mackow E. R., Dyall-Smith M. L., Lazdins I., Holmes I. H., Greenberg H. B. Serotypic analysis of VP3 and VP7 neutralization escape mutants of rhesus rotavirus. J Virol. 1988 Sep;62(9):3509–3512. doi: 10.1128/jvi.62.9.3509-3512.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shaw R. D., Stoner-Ma D. L., Estes M. K., Greenberg H. B. Specific enzyme-linked immunoassay for rotavirus serotypes 1 and 3. J Clin Microbiol. 1985 Aug;22(2):286–291. doi: 10.1128/jcm.22.2.286-291.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shaw R. D., Vo P. T., Offit P. A., Coulson B. S., Greenberg H. B. Antigenic mapping of the surface proteins of rhesus rotavirus. Virology. 1986 Dec;155(2):434–451. doi: 10.1016/0042-6822(86)90205-9. [DOI] [PubMed] [Google Scholar]
- Starkey W. G., Collins J., Wallis T. S., Clarke G. J., Spencer A. J., Haddon S. J., Osborne M. P., Candy D. C., Stephen J. Kinetics, tissue specificity and pathological changes in murine rotavirus infection of mice. J Gen Virol. 1986 Dec;67(Pt 12):2625–2634. doi: 10.1099/0022-1317-67-12-2625. [DOI] [PubMed] [Google Scholar]
- Svennerholm A., Lange S., Holmgren J. Correlation between intestinal synthesis of specific immunoglobulin A and protection against experimental cholera in mice. Infect Immun. 1978 Jul;21(1):1–6. doi: 10.1128/iai.21.1.1-6.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Svensson L., Sheshberadaran H., Vesikari T., Norrby E., Wadell G. Immune response to rotavirus polypeptides after vaccination with heterologous rotavirus vaccines (RIT 4237, RRV-1). J Gen Virol. 1987 Jul;68(Pt 7):1993–1999. doi: 10.1099/0022-1317-68-7-1993. [DOI] [PubMed] [Google Scholar]
- Taniguchi K., Hoshino Y., Nishikawa K., Green K. Y., Maloy W. L., Morita Y., Urasawa S., Kapikian A. Z., Chanock R. M., Gorziglia M. Cross-reactive and serotype-specific neutralization epitopes on VP7 of human rotavirus: nucleotide sequence analysis of antigenic mutants selected with monoclonal antibodies. J Virol. 1988 Jun;62(6):1870–1874. doi: 10.1128/jvi.62.6.1870-1874.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Taniguchi K., Morita Y., Urasawa T., Urasawa S. Cross-reactive neutralization epitopes on VP3 of human rotavirus: analysis with monoclonal antibodies and antigenic variants. J Virol. 1987 May;61(5):1726–1730. doi: 10.1128/jvi.61.5.1726-1730.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Taniguchi K., Urasawa T., Kobayashi N., Ahmed M. U., Adachi N., Chiba S., Urasawa S. Antibody response to serotype-specific and cross-reactive neutralization epitopes on VP4 and VP7 after rotavirus infection or vaccination. J Clin Microbiol. 1991 Mar;29(3):483–487. doi: 10.1128/jcm.29.3.483-487.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Van Loveren H., Osterhaus A. D., Nagel J., Schuurman H. J., Vos J. G. Detection of IgA antibodies and quantification of IgA antibody-producing cells specific for ovalbumin or Trichinella spiralis in the rat. Scand J Immunol. 1988 Sep;28(3):377–381. doi: 10.1111/j.1365-3083.1988.tb01463.x. [DOI] [PubMed] [Google Scholar]
- Van der Heijden P. J., Bianchi A. T., Stok W., Bokhout B. A. Background (spontaneous) immunoglobulin production in the murine small intestine as a function of age. Immunology. 1988 Oct;65(2):243–248. [PMC free article] [PubMed] [Google Scholar]
- Vesikari T., Kapikian A. Z., Delem A., Zissis G. A comparative trial of rhesus monkey (RRV-1) and bovine (RIT 4237) oral rotavirus vaccines in young children. J Infect Dis. 1986 May;153(5):832–839. doi: 10.1093/infdis/153.5.832. [DOI] [PubMed] [Google Scholar]
- Ward R. L., Knowlton D. R., Greenberg H. B., Schiff G. M., Bernstein D. I. Serum-neutralizing antibody to VP4 and VP7 proteins in infants following vaccination with WC3 bovine rotavirus. J Virol. 1990 Jun;64(6):2687–2691. doi: 10.1128/jvi.64.6.2687-2691.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ward R. L., Knowlton D. R., Schiff G. M., Hoshino Y., Greenberg H. B. Relative concentrations of serum neutralizing antibody to VP3 and VP7 proteins in adults infected with a human rotavirus. J Virol. 1988 May;62(5):1543–1549. doi: 10.1128/jvi.62.5.1543-1549.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wilson A. D., Clarke C. J., Stokes C. R. Whole cholera toxin and B subunit act synergistically as an adjuvant for the mucosal immune response of mice to keyhole limpet haemocyanin. Scand J Immunol. 1990 Apr;31(4):443–451. doi: 10.1111/j.1365-3083.1990.tb02791.x. [DOI] [PubMed] [Google Scholar]
- Wolf J. L., Dambrauskas R., Sharpe A. H., Trier J. S. Adherence to and penetration of the intestinal epithelium by reovirus type 1 in neonatal mice. Gastroenterology. 1987 Jan;92(1):82–91. doi: 10.1016/0016-5085(87)90842-0. [DOI] [PubMed] [Google Scholar]
- Wolf J. L., Rubin D. H., Finberg R., Kauffman R. S., Sharpe A. H., Trier J. S., Fields B. N. Intestinal M cells: a pathway for entry of reovirus into the host. Science. 1981 Apr 24;212(4493):471–472. doi: 10.1126/science.6259737. [DOI] [PubMed] [Google Scholar]
- Woode G. N., Zheng S., Melendy D. R., Ramig R. F. Studies on rotavirus homologous and heterologous active immunity in infant mice. Viral Immunol. 1989;2(2):127–132. doi: 10.1089/vim.1989.2.127. [DOI] [PubMed] [Google Scholar]